World Journal of
WJ C C
Submit a Manuscript: https://www.f6publishing.com
DOI: 10.12998/wjcc.v7.i20.3202
Retrospective Study
Rh-incompatible hemolytic disease of the newborn in Hefei
Shao-Hua Bi, Liang-Liang Jiang, Li-Ying Dai, Hong Zheng, Jian Zhang, Li-Li Wang, Chao Wang, Qiao Jiang,
Yu Liu, Yong-Li Zhang, Juan Wang, Chao Zhu, Guang-Hui Liu, Ru-Jeng Teng
ORCID number: Shao-Hua Bi
(0000-0001-5844-3072); Liang-Liang
Jiang (0000-0001-7624-0439); Li-
Ying Dai (0000-0003-3914-9155);
Hong Zheng (0000-0002-5437-4193);
Jian Zhang (0000-0001-5218-003X);
Li-Li Wang (0000-0002-1134-0559);
Chao Wang (0000-0002-5492-5127);
Qiao Jiang (0000-0001-6568-0471);
Yu Liu (0000-0002-4573-9090);
Yong-Li Zhang
(0000-0001-7878-7630); Juan Wang
(0000-0001-7184-9085); Chao Zhu
(0000-0002-6467-2071); Guang-Hui
Liu (0000-0002-1682-6187); Ru-Jeng
Teng (0000-0003-4321-2452).
Author contributions: Bi SH and
Teng RJ designed the research; Bi
SH, Liu GH, and Teng RJ drafted
the manuscript; Bi SH, Jiang LL,
Dai LY, Zheng H, Zhang J, Liu Y,
Zhang YL, and Wang J obtained
the informed consents reviewed
the medical records; Wang C and
Jiang Q performed the laboratory
tests; Bi SH, Zhu C, Liu GH, and
Teng RJ performed the data
analysis; Wang LL, Zhu C, Liu GH,
and Teng FJ revised the
manuscript; Bi SH, Zhu C, Liu GH,
and Teng RJ finalized the
manuscript.
Institutional review board
statement: See uploaded file for
IRB approval in Chinese.
Conflict-of-interest statement: The
authors report no relevant conflicts
of interest.
Data sharing statement:
Deidentified raw data can be
obtained from the authors upon
official request for research
purpose only.
WJCC https://www.wjgnet.com
Clinical Cases
World J Clin Cases 2019 October 26; 7(20): 3202-3207
ISSN 2307-8960 (online)
ORIGINAL ARTICLE
Shao-Hua Bi, Li-Ying Dai, Hong Zheng, Jian Zhang, Yu Liu, Yong-Li Zhang, Juan Wang, Guang-
Hui Liu, Divisions of Neonatology, Anhui Provincial Children’s Hospital, Hefei 230022, Anhui
Province, China
Liang-Liang Jiang, Pediatrics Neurology, Anhui Provincial Children’s Hospital, Hefei 230022,
Anhui Province, China
Li-Li Wang, Chao Zhu, Division of Neonatology, First Affiliated Hospital of Anhui Medical
University, Hefei 230022, Anhui Province, China
Chao Wang, Hefei Blood Center, Hefei 230022, Anhui Province, China
Qiao Jiang, Clinical pathology, Anhui Provincial Children’s Hospital, Hefei 230022, Anhui
Province, China
Ru-Jeng Teng, Division of Neonatology, Department of Pediatrics, Medical College of
Wisconsin, Milwaukee, WI 53226, United States
Corresponding author: Guang-Hui Liu, MD, Chief Doctor, Division of Neonatology, Anhui
Provincial Children’s Hospital, Anhui Medical University, Wangjiang E. Rd, Hefei 230022,
Anhui Province, China. lgh508@sina.com
Telephone: +86-551-62237807
Abstract
BACKGROUND
Anti-D antibody is not the common cause of Rh-isoimmunization in Chinese
neonatal jaundice. Recent change in national population policy has followed by
an increase in Rh-isoimmunization related hemolytic disease of the newborn
(HDN). Unfortunately, regional status of Rh-HDN is unavailable. We
hypothesize that Rh-HDN in our region is most commonly due to anti-E
antibody.
AIM
To investigate the prevalence of hemolytic disease of the newborn due to Rh-
isoimmunization in Hefei City.
METHODS
Retrospective review of data obtained from Children’s Hospital of Anhui and
Hefei Blood Center between January 2017 and June 2019. Status of minor blood
group antibody was studied in the corresponding mothers.
RESULTS
Totally 4138 newborns with HDN admitted during the study period and 116
3202 October 26, 2019 Volume 7 Issue 20

Open-Access: This article is an
open-access article which was
selected by an in-house editor and
fully peer-reviewed by external
reviewers. It is distributed in
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Commons Attribution Non
Commercial (CC BY-NC 4.0)
license, which permits others to
distribute, remix, adapt, build
upon this work non-commercially,
and license their derivative works
on different terms, provided the
original work is properly cited and
the use is non-commercial. See:
http://creativecommons.org/licen
ses/by-nc/4.0/
Manuscript source: Unsolicited
manuscript
Received: July 23, 2019
Peer-review started: July 23, 2019
First decision: September 9, 2019
Revised: September 22, 2019
Accepted: October 5, 2019
Article in press: October 5, 2019
Published online: October 26, 2019
P-Reviewer: Aydin M,
Govindarajan GK
S-Editor: Zhang L
L-Editor: Filipodia
E-Editor: Qi LL
WJCC https://www.wjgnet.com
Bi SH et al. Rh-HDN in Chinese
(2.8%) received blood exchange transfusion (BET). Eighteen newborns (0.43%)
with proven Rh-incompatible HDN were identified. All were not the first-born
baby. Thirteen mothers were RhD (+) (72%) and five were RhD (-). The
distribution of Rh-related antibodies in mothers was ten anti-E (55%), five anti-D
(27%), and for one anti-C, anti-c, and anti-E/c (6%) each. Thirteen (72.2%) were
qualified for BET, relative risk for BET was 28.9 as compared to other types of
HDN, but only 10 received due to parenteral refusal. All (100%) RhD related
HDN received BET which is not significantly different from RhE related HDN
(81.8%).
CONCLUSION
As expected, all Rh-incompatible HDN newborns were not the first-born.
Contrary to the Caucasian population, anti-D induced HDN is not the most
common etiology. In our region, anti-E (11/18, 61%) is the most common cause of
Rh-HDN.
Key words: Rh-isoimmunization; Hemolytic disease of the newborn; Minor blood group
©The Author(s) 2019. Published by Baishideng Publishing Group Inc. All rights reserved.
Core tip: Rh-hemolytic disease of the newborn (HDN) is more commonly seen after the
change of national population policy in China. Different from Caucasian, the most
common antibody that causes Rh-HDN in Chinese neonates is the anti-E antibody. The
severity of anti-E Rh-HDN seems no less than anti-D Rh-HDN since most of our
indexed cases were qualified for blood exchange transfusion. This emerging medical
problem requires a nationwide collaboration of research in order to establish evidence-
based guidelines for Chinese population.
Citation: Bi SH, Jiang LL, Dai LY, Zheng H, Zhang J, Wang LL, Wang C, Jiang Q, Liu Y,
Zhang YL, Wang J, Zhu C, Liu GH, Teng RJ. Rh-incompatible hemolytic disease of the
newborn in Hefei. World J Clin Cases 2019; 7(20): 3202-3207
URL: https://www.wjgnet.com/2307-8960/full/v7/i20/3202.htm
DOI: https://dx.doi.org/10.12998/wjcc.v7.i20.3202
INTRODUCTION
Hemolytic disease of the newborn (HDN), or erythroblastosis fetalis, is due to blood
type incompatibility between the mother and the fetus. This incompatibility causes
the mother’s immune system to generate IgG antibody against the blood type of the
fetus. The IgG antibody binds to fetal red blood cells transplacentally to cause
hemolysis. ABO isoimmunization is the most common etiology for HDN but minor
blood group isoimmunization can also cause severe HDN. Different from ABO-HDN,
minor blood group HDN usually will not occur in the first-born newborn unless the
mother has prior abortion, inadequate transfusion, or miscarriage. During the era of
one-child policy, we had extremely limited experience with minor blood group HDN.
There were only a few reports about minor blood group HDN in China[1-3]. After
discontinuation of the one-child policy, we believe that pediatricians will start to
experience more minor blood group HDN.
Our clinical experience tells us that Rh-isoimmunization is the second most
common cause of HDN in Chinese newborns[1,3]. Without early recognition, Rh-HDN
can cause severe neonatal jaundice that can complicate with kernicterus or death.
Severe Rh-HDN can also lead to fetal demise, miscarriage, or premature birth.
Neutropenia and thrombocytopenia can be a clinical manifestation of newborns with
Rh-HDN[4,5]. Occasionally, the fetal hydropic change can cause uterine atony, maternal
preeclampsia, mirror (Ballantyne) syndrome[6], or difficulty in cross-matching. Early
identification of the at-risk pregnancy and intrauterine intervention may offer a better
outcome of the newborn and the mother. After the introduction of Rhogam in the
1960, problems from Rh-isoimmunization are almost eradicated[7]. However, we do
not know whether Rhogam can offer similar benefit to our population or not. Up-to-
now, our medical society still lacks adequate data to guide us to develop a rational
management pathway. Our study is aimed to call for the attention to Rh-HDN in
3203 October 26, 2019 Volume 7 Issue 20
Bi SH et al. Rh-HDN in Chinese

Chinese population.

MATERIALS AND METHODS

We prospectively initiated a collaboration between Anhui Provincial Children’s
Hospital and Hefei Blood center for this cohort study. Blood types of parents and the
newborns, hemolysis, and antibodies of minor blood groups were tested for all
newborns admitted for neonatal jaundice. Both coagulated and anti-coagulated blood
from mother and newborn was collected according to the Chinese National
Standardized Protocols for Clinical Laboratory, 4th version, for saline cross matching,
polybrene test, and Coombs test. Antibodies against Rh group including anti-D, anti-
E, anti-e, anti-C, and anti-c were tested together with ant-A and anti-B. Blood was also
tested for hemoglobin, non-specific antibody, reticulocyte count, direct Coombs test,
and indirect Coombs test. The study started from January 2017 to June 2019. Consent
for data collection was obtained from the parents. Due to limited case numbers, non-
parametric test was used for comparisons between two groups. Fisher’s exact test was
used to compare categorical data between two groups. Data were analyzed by Prism 8
for Windows v.8.1.2.

RESULTS
Our hospital adopted the American Academy of Pediatrics guidelines published in
2004 to diagnose and manage neonatal jaundice[8]. During the study period there were
totally 4138 newborns admitted for neonatal hyperbilirubinemia and 116 (2.8%) of
them received double-volume blood exchange transfusion (BET). There were totally
18 mother-newborn dyads in our study (0.4%) without ABO incompatibility. Among
those 18 mothers, 3 were blood type A, 6 were blood type B, 5 were blood type O, and
4 were blood type AB. Thirteen mothers were RhD (+) and 5 were RhD (-) (Table 1).
Direct Coombs test, free antibody test, and antibody release test were positive for all
18 index cases. Thirteen out of the 18 newborns (55.6%) were qualified for BET but 3
of them did not undergo the procedure due to refusal by their parents. This left only
10 newborns received BET which accounted for 8.6% of all newborns who received
BET during the study period. Rh-HDN had much higher risk to be qualified for BET
(relative risk = 28.9, odds ratio = 101.4; P < 0.0001 by Fisher exact test). All 3 newborns
qualified for BET but did not receive the procedure were born to RhD (+) mothers
with anti-E antibody. Among the 10 newborns received BET, all five newborns from
RhD (-) mothers as compared to 5 from RhD (+) mothers. There was no difference in
the percentage of requiring BET between newborns from RhD (-) mothers and RhD
(+) mothers (5/5 versus 8/13, P = 0.25 by Fisher exact test). All 10 newborns tolerated
the exchange transfusion and discharged home without complication. Fifteen
newborns (83.3%) were the 2nd born while 3 (16.7%) were the 3rd born. The reticulocyte
counts ranged between 1.12% and 25.3%. Though the median reticulocyte count was
higher for newborns from RhD (-) mothers (18.53% versus 8.37%), the difference was
not statistically significant (P = 0.40). There were 10 mothers with E antibody (55%), 5
with anti-D antibody (27%), one with both anti-E and anti-c antibodies (6%), and one
each for anti-C (6%) and anti-c antibody (6%).

DISCUSSION
Blood group isoimmunization has been known to be a major cause of hydrops fetalis
since 1940s[9] and the most important cause of neonatal jaundice[8]. The most common
etiology of blood group isoimmunization is ABO-isoimmunization while Rh-
isoimmunization is the second most common etiology. However, before the
introduction of Rhogam, Rh-isoimmunization used to be the most common cause of
kernicterus[9]. After exposure to fetal blood with different blood type the maternal
immune system can be sensitized to generate IgG antibody, an isotype that can cross
placenta into fetal circulation, to hemolyze fetal red blood cells[10]. The introduction of
postpartum Rhogam injection has successfully reduce the Rh (D) sensitization from
14% down to 1%-2% and the addition of antepartum Rhogam injection further
reduces the sensitization down to 0.5%[11]. Unfortunately, the successful experience
cannot apply to our population for since less than 1% of pregnant women is RhD (-).
Although Rh-HDN only accounted for less than 1% (0.43%) of all HDN admission
in hour hospital, the relative risk for requiring BET was 28.9-fold of other type of
HDN. With roughly 7 cases per year (18 cases over 2.5 years) in our hospital, Rh-HDN

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 Bi SH et al. Rh-HDN in Chinese

Table 1 Blood group information of the parents and the newborn, maternal pregnancy status, and laboratory data of the newborns

Direct Reti- Gesta-

Free Anti- Direct-
Blood Blood Blood Coo- Minor culo- tional T-bil Hb
anti- body Ges- bil
Case type type type mbs blood BET Rh (D) cyte age Age (µmol/
body- relea- tation (µmol/
(F) (M) (N) group count (wee- L)
test test setest L) (g/L)
(%) ks)

1 O O O + + + E Y - G3P3 4.10 41+0 5d 406.1 100.8 133

1
2 O B B + + + E N + G4P2 4.50 39+5 33h 370.7 20.1 145
3 O O O + + + D Y - G5P2 19.17 39+3 25h 326.6 66.3 74
4 A B AB + + + E N + G5P2 11.99 38+6 3d 361.0 30.0 105
+1
5 A A A + + + E, c Y + G3P2 18.25 37 24h 469.3 30.5 83
6 B A AB + + + E Y + G3P2 25.30 40+3 32h 471.1 75.6 76
7 A B A + + + E N1 + G3P2 3.95 37+6 3d 407.0 18.1 208
8 O O O + + + D Y - G3P3 3.63 40+6 5d 365.7 28.7 120
+2
9 A AB AB + + + E N + G2P2 1.12 40 8d 228.9 21.4 122
10 O AB B + + + D Y + G4P3 8.07 39+0 20h 282.1 33.1 137
11 A B B + + + E Y + G4P2 22.97 38+4 11h 257.4 28.1 97
1 +4
12 O O O + + + E N + G2P2 15.62 39 21h 347.9 16.3 121
13 O O O + + + C N + G2P2 12.20 39+2 3d 275.4 10.0 106
14 A B AB + + + D Y - G2P2 18.53 40+0 10h 249.9 14.6 113
15 O AB B + + + E Y + G2P2 8.67 39+2 10h 447.4 21.3 93
+6
16 A B B + + + c N + G2P2 2.88 37 6d 312.5 32.4 160
17 A A A + + + D Y - G2P2 18.53 39+4 14h 292.4 26.2 105
18 B AB B + + + E N + G3P2 4.50 39+0 3d 288.6 21.5 138

1
Newborn received intensive phototherapy after meeting threshold of BET due to refusal by parents. F: Father; M: Mother; N: Newborn; BET: Blood
exchange transfusion; T-bil: Total bilirubin.

is not an uncommon problem we are facing. Rh blood group system is one of the
more than 40 known human blood group systems. There are two sets of
nomenclatures for Rh blood group, one developed by Fisher et al[12] and the other by
Wiener[13]. The Fisher system is more commonly used by clinicians which contains 3
classes of epitope (C, c, D, d, E, e) and are encoded by two adjacent gene loci on
chromosome 1. Due to their proximity on the DNA, the 3 classes of epitope co-express
in a complex pattern with at least 34 genotypes. The potency of antigenicity studied
show D > E > C > c > e > d which explains the severity of neonatal jaundice caused by
the corresponding antibody.
As compare to ABO-HDN, the Rh-HDN has more aggressive hemolysis as reflected
by more of the patients require BET. It is believed that fetal red blood cell (RBC)
express less A/B antigen on the cell membrane and A/B antigen also express on other
cell types which can decrease the binding of antibody to the RBC.
The D gene (D or d) is located on short arm (p) of chromosome 1 with 94%
population as RhD (+) and 6% RhD (-) globally. Caucasian has the highest (15%) RhD
(-) than Black (8%) and Asian population (< 1%) [14] which makes the Rh (D)
isoimmunization extremely rare in Chinese population. C (C or c) and E (E or e) are
co-express due to their proximity. The genotype distribution of C (68%Caucasian,
27%Black, and 93%Asian), c (80%Caucasian, 96%Black, and 47%Asian), E
(29%Caucasian, 22%Black, and 39%Asian), and e (98%Caucasian, 98%Black, and
96%Asian)[15] is in agreement with the previous reports suggest isoimmunization
against E and c is more common in the Chinese population[1,3]. In our results, only 5
HDN were associated with anti-D antibody. However, all 5 HDN with anti-D
antibody received BET as compared to 8 out of 13 (61.5%) in anti-D negative
newborns who qualified for BET although 3 did not receive it due to parenteral
refusal.
Since Rh-HDN is very rare in Chinese population and rarely occurs in the first
pregnancy, unless there was a prior abortion or miscarriage, so our medical
community really lacks the knowledge of this morbidity especially during the one-
child policy era. Rh (D) mediated HDN is just one kind of the Rh-HDN which can be
prevented or managed by Rhogam. Unfortunately, there is no role for Rhogam in C, c,
E, e antibody mediated HDN. With the recent reversion of one-child policy we can
expect the number of CcEe-mediated HDN may increase and we need to prepare for

WJCC https://www.wjgnet.com 3205 October 26, 2019 Volume 7 Issue 20

Bi SH et al. Rh-HDN in Chinese

this change. We pediatricians need to be aware that Rh (+), as we commonly call for
those RhD (+) pregnant women, do not guarantee that there is no risk for their
newborns to develop Rh-HDN. We also need to know that first-born newborn is not
completely protected from Rh-HDN if the mother had prior abortion, transfusion, or
miscarriage. Our obstetric colleagues are recommended to provide at least 500 I.U.
Rhogam injection to pregnant women at 28 wk’ and 34 wk’ gestation, or one 1500 I.U.
injection at 28 wks’ gestation, to RhD (-) pregnant women, followed by a 500 I.U.
injection within 72 h after delivery to prevent Rh (D) sensitization if they are Rh (D)-
negative with a Rh (D)-positive sex partner.
In the presence of ABO incompatibility, the chance to develop Rh sensitization
decreases dramatically by at least 2.4-fold[16]. This protective effect is believed to come
from the higher antigenicity of the ABO blood group. It is interesting that none of our
newborns complicated with ABO incompatibility, but clinical significance deserves
more extensive multi-institutional studies in the future. During clinical work-up,
caution needs to be paid for that direct Coombs test can be negative in severe Rh-
HDN due to extremely high titer of the antibody[17]. Contrary to Rhogam, Anti-E
antibody is presently not available for preventing and treating anti-E mediated HDN.
However, non-specific intravenous immunoglobulin can be used to ameliorate the
severity of hemolysis and hence the jaundice[18].
In conclusion, Rh-HDN is an infrequent cause of HDN but can elicit severe
hemolysis. In the present era, we need to be more familiar with the spectrum of this
disease since most of our Rh-HDN is not due to anti-D antibody and cannot be
prevented by the Rhogam injection. Our results only represent our regional
experience. An extensive collaboration between pediatrician, obstetricians, and
transfusion experts is required for a better understanding of Rh-HDN that can help us
to establish a proper guideline in management.

ARTICLE HIGHLIGHTS
Research background
Before the discontinuation of the national population policy one-child policy–Rh-hemolytic
disease of the newborn (HDN) was a rare cause of severe neonatal jaundice in China. Different
from Caucasian population, RhD (-) is extremely rare in Chinese. We experienced a dramatical
increase in Rh-HDN since the discontinuation of the national population policy which we
believe will impact our management of neonatal jaundice nationwide. The lack of our own
epidemiologic data will hinder our generation of public health policy judging from the severe
consequence of bilirubin induced neurologic deficit.

Research motivation
To share our experience with our colleagues to encourage a statewide or nationwide
collaboration to study Rh-HDN in Chinese.

Research objectives
The investigate the distribution of Rh antibodies in Chinese HDN and the clinical manifestation.

Research methods
Retrospective chart review of prospectively collected cohort over 18 mo in one free standing
Children’s Hospital.

Research results
Rh-HDN accounted for 0.43% (18 out of 4138) of all HDN and 72.2% (13/18) were qualified for
BET. No mother received antenatal Rhogam injection. The most common antibody involved was
anti-E (55%, 10/18). The risk for BET was similar between anti-D (100%) and anti-E (81.8%) Rh-
HDN.

Research conclusions
Anti-E antibody is the most common cause of Rh-HDN in Chinese. Our limited experience
showed the severity of RhE neonatal jaundice is no less severe than the RhD neonatal jaundice.

Research perspectives
More extensive study in Rh-HDN is warranted after the change of our national population
policy. The severity of Rh-HDN to both pregnant women and fetus deserve our attention.
Collaboration among perinatology, neonatology, hematology, and immunology is needed to
provide the best care for our next generation.

ACKNOWLEDGEMENTS
Thanks for all the nursing staff, medical technicians, and medical informatics of the

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 Bi SH et al. Rh-HDN in Chinese

Anhui Provincial Children’s Hospital and Hefei Blood Center. Without their help this
study cannot be accomplished.

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